The advent of animals: The view from the Ediacaran

The Temporal and Spatial Record

Fossils of the Ediacara biota occur at 40 localities worldwide, with four particularly good localities; namely, southeastern Newfoundland, the Flinders Ranges of South Australia, the White Sea Region of Russia, and Namibia (2, 16). The Ediacara fossil assemblages have traditionally been demarcated as three successive assemblages: the Avalon, the White Sea, and the Nama, which have been interpreted as a reflection of evolutionary controls, as evidenced by the radiometric ages of several key localities (2). However, there are also strong secondary preservational (17, 18) and paleoenvironmental controls (19, 20).

What is apparent is that the older Avalon Assemblage contains a distinct assemblage of taxa that exhibit only a few broad morphologic [e.g., rangeomorphs and arboreomorphs (cf. 21)] types. Particularly striking are the common fractal-like self-similar branching rangeomorph forms with surface area/volume ratios, which are comparable to modern osmotrophic bacteria. Although this feeding type is restricted to these bacteria in the modern era, these self-similar growths may have represented a strategy for overcoming physiologic constraints that typically make osmotrophy prohibitive for macroscopic life forms (22). Further, these early unusual and distinct macroorganisms may have been important in cycling dissolved organic carbon that may have been abundant in the Ediacaran times (22).

Elements of the Avalon Assemblage persisted (19, 21), but there are major increases in biologic and ecologic complexity following in the wake of the appearance of the older Avalon Assemblage that more strongly relate to animals as we understand them. The younger, “second wave” of the Ediacara Biota comprising the White Sea and Nama assemblages includes a wide range of new taxa (Fig. 1) (2, 21) that exhibit pronounced biologic and ecologic innovation, as evidenced by dramatic increases in body plans and ecospace use; it is a radiation in its own right. Notable aspects of this radiation include dramatic increases in mobility (18); the appearance of undisputed bilaterians, such as burrowing organisms and stem-group mollusks (e.g., refs. 23 and 24); the advent of sexual reproduction (25); the appearance of the first biomineralizers (26, 27); and the advent of active heterotrophy by multicellular organisms (24, 28⇓–30, 31).

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Fig. 1.

Common Ediacara biota fossils from the Ediacara Member, Rawnsley Quartzite, Flinders Ranges, South Australia. (A) Dickinsonia costata with precontraction outline. (B) Funisia dorothea preserved as body casts and external molds where casts have been lost. (C) Two specimens of Parvancorina minchami. (D) Kimberella quadrata. (E) Multilayered sandstone case of Bradgatia sp. (F) Sandstone cast of scratch traces, Kimberichnus teruzzii, produced by K. quadrata. (G) Spriggina floundersi. (H) Internal cast of three walls of Pteridinium simplex. (I) Helminthoidichnites isp., groove and levee traces preserved on a bed base. Specimens D and G are from the Ediacara Conservation Park; other specimens are from the Nilpena Heritage Site. (Scale bar: 1 cm.)

Moreover, this diversification in macrofauna body plans and ecologies was accompanied by a diversification in organically bound microbial substrates (microbial mats) recorded in the form of extensive sedimentary textures both physically and biologically mediated. These textured organic surfaces (TOS) are diverse patterned assemblages of structures that partially or completely cover bedding surfaces. Lacking autonomous taxonomic traits, they nonetheless possess discrete, repeating characters (11, 32). The constituent organisms may have been members of a prokaryotic, microbial community. However, it is likely that they were eukaryotic forms (32) and that certain large and multicomponent TOS may actually consist of assemblages of multicellular body fossils (25, 32). Regardless of phylogenetic affinity, TOS played a distinctive role in Ediacara seafloor ecology, both as members of Ediacara communities and likely as preservational mediators (17).

Although TOS are known from Avalon fossil assemblages (33), they achieved unprecedented abundance, morphologic diversity, and complexity as part of the second wave radiation (32). Many of the new body and trace fossil taxa characteristic of second wave assemblages occur in intimate association with TOS and appear to represent matground-based, heterotrophic lifestyles.

Environments of the Ediacara Biota

There are abundant data and general consensus that all the deposits that bear Ediacara fossils are marine in origin (19, 34). Although a terrestrial origin was recently proposed (35), this hypothesis has been rigorously tested and is not consistent with any of the sedimentologic data (31, 34, 36⇓⇓⇓–40). Fossils of the Ediacara Biota are indeed preserved in a variety of marine environments (2), from outer shelf and slope settings in volcanic sediments of forearc basins of the Avalon Terrane (41, 42) to prograding carbonate platforms such as southern China (43, 44) and shallow marine prograding siliciclastic environments of the east European Platform (19, 20, 45, 46). Burial events enabled samples of benthic communities to be conserved that included sessile body fossils and trace fossils. However, these snapshots also include elements of the history of each surface, beginning with recruitment of benthic taxa (18, 25), ambient currents and wave events, ecologic succession (47), degradation of organisms, and evidence of current deformation and loss of sessile frondous forms in the final burial event (48, 49).

Within each Ediacaran assemblage there are considerable differences in the biotic composition, depending on wave energy, the sedimentary substrate, and the depth of benthic communities (19, 20). As a consequence, the most useful field exposures are those in which whole bedding surfaces can be exposed and studied from differing paleoenvironmental settings within a region, particularly in field sites where multiple specimens and surfaces can be excavated and studied, such as the coastal exposure in eastern Newfoundland, the White Sea region of northwestern Russia, the Nilpena site in the Flinders Ranges of South Australia, and the Aar Farm site in southern Namibia.

Heterogeneity of the Ediacaran Seafloor: An Example from the Ediacaran of South Australia

One of the defining characteristics of the Ediacara Biota fossils is that they are typically preserved in situ. As a result, extensive bedding planes preserve individual communities as accurately as is possible in the fossil record. The Flinders Ranges region of South Australia contains one of the best-exposed and most complete successions of Neoproterozoic to early Paleozoic rocks in the world and includes the type section for the Ediacaran Period. Ediacara fossils occur within the Ediacara Member of the Rawnsley Quartzite, preserved within a succession of shallow marine and deltaic facies and representing common components of the White Sea Assemblage.

Well-known fossils of the Ediacara Member, including Dickinsonia (Fig. 1A), Kimberella (Fig. 1D), Parvancorina (Fig. 1C), Spriggina (Fig. 1G), and other taxa, occur abundantly on the base of thin-bedded rippled quartz sandstones representing deposition in shallow marine settings between fair-weather and storm wave base. The rich fossil assemblages of this wave-base sand facies represent benthic communities typically smothered by sand deposited by waning storm surges. Fossils are also preserved on the base of the beds of the sheet-sand facies, where fluidized sand smothered benthic communities in deeper water, well below wave base.

Excavation of 28 fossiliferous beds 4–25 m² in area within these two facies demonstrates marked heterogeneity in both abundance and diversity between beds (Fig. 2). Within each facies, successions of beds of nearly identical sedimentology suggest the possibility there was “community-scale” differentiation of taxa in the Ediacara ecosystem, where taxa were responding to small-scale changes in environmental conditions, resulting in a patchy distribution of taxa. These bedding plane data provide an unusually good opportunity to examine abundance diversity relationships, as time-averaging can be assumed to be as minimal as possible. Rarefied generic diversity curves indicate considerable variation between beds, but overall, the wave-base facies has a greater diversity overall than the sheet-sands facies (Fig. S1). Individual beds of the Ediacara Member exhibit a wide range of evenness values (Fig. S2). Although beds with low evenness and high dominance are not rare, there are beds with evenness values on par with those of the Phanerozoic. Furthermore, although these data are not similarly collected, the results are consistent with the suggestion of Powell and Kowalewski (50) that evenness increases through time (Fig. S2). In most Ediacaran cases, the same taxa are present on most of the beds, but it is the varying abundances of each that characterize these assemblages. For example, Dickinsonia and the frond holdfast Aspidella both occur on nearly all of the beds, but in some cases, Dickinsonia dominates beds and in others, Aspidella dominates, indicating the presence of abundant frondose organisms.

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Fig. 2.

The relative abundance of different fossils on the excavated beds from South Australia. The total number of fossils found on the bed is given in parentheses after the bed name. All the beds shown, with the exception of the beds represented by the four right columns, represent deposition between fair-weather and storm wave base [the wave-base sand facies of Gehling and Droser (19)]. The four beds on the right are within the sheet-flow sand facies. The body fossil Funisia is preserved on beds MM2, Matt, and STC-X in abundances that range in the thousands, and thus, these fossils actually dominate beds. However, their dense packing and typically poor preservation do not allow for accurate counts on these beds.

Both the bed heterogeneity data and evenness values show that even though these represent nearly the oldest animal communities (following on the heels of those of the Avalon Assemblage), there is a sophistication of community assembly on par with that of the Phanerozoic. This is striking, considering the lack of evidence for predation, infaunalization, and widespread skeletonization. Although there is little evidence of interactions between taxa, there are abundant indications that several of the taxa were interacting with the mat.

Population Structure and Reproduction

Preservation of extensive bedding planes also permits analysis of large numbers of a single taxon in situ. Funisia dorothea (Fig. 1B) occurs in huge abundance on a number of bedding planes. It is up to 30 cm long and 12 mm in diameter and is divided longitudinally into serial units 6–8 mm in length throughout the length of the tube (Fig. 1B). Units within the tube decrease in width progressively toward the apex, suggestive of growth via terminal addition. Individuals can occur within dense assemblages, sometimes greater than 1,000/m². Funisia tubes are directly connected to attachment structures that range from 1 to 8 mm. Importantly, attachment structures of a similar size and developmental stage are spatially clustered, even within individual bedding surfaces.

The phylogenetic affinity of F. dorothea is problematic. The lack of evidence for polypoid openings or pores in the body wall limits our understanding of its taxonomic affinities. However, although it is difficult to place these fossils within Metazoa, the morphology and ecology are suggestive of cnidarian or poriferan grade animals. The branching patterns and rarity of branching of Funisia is consistent with metazoan asexual budding. The consistency of tube widths on individual bedding surfaces, the densely packed nature of the attachment structures, and the clustering pattern of developmental stages of attachment structures on individual bedding planes suggests the juveniles settled as aggregates in a series of limited cohorts.

These solitary organisms thus exhibit growth by the addition of serial units to tubes and by the division of tubes, and dispersed propagation via the production of spats. Among living organisms, spat production is almost ubiquitously the result of sexual reproduction but is known to occur rarely in association with asexual reproduction. Hence, despite its morphologic simplicity, the F. dorothea provides evidence of a variety of growth modes and a complex arrangement for the propagation of new individuals.

Aggregation is not uncommon among some elements of the Ediacara biota, being present in the frondose holdfast Aspidella. These typically occur in dense assemblages, but in contrast to F. dorothea, their right skewed size distribution is consistent with continuous recruitment, rather than being periodic (18). Recently, Darroch and colleagues (51) analyzed the population structures of three rangeomorph taxa and one nonrangeomorph from Mistaken Point, using the Bayesian Information Criterion likelihood-based model selection. They found that although the populations of these taxa had wide distributions, each population was best described as a single distribution. The authors suggest that, assuming these organisms reproduced sexually, their findings most strongly support a continuous or year-round reproduction strategy for these taxa, as this would allow for unimodal populations with large overall size ranges.

Only a few studies of large numbers of individual taxa preserved on a single bedding plane have been done. However, with continued excavation at various sites, these types of studies have the promising potential to elucidate the biology of these organisms, if not the phylogeny, providing another step toward understanding the link with Cambrian and younger animals.

Skeletonization and a Link to the Cambrian

The apparent lack of taxonomic continuity between the Precambrian and Cambrian fossil records has led to controversial and conflicting interpretations about the Ediacara biota and their place in the evolution of metazoan life on this planet. This has been further complicated by the absence of similar modes of construction between these faunas and the rarity of Precambrian skeletonized fossils. A relatively new Ediacara fossil, Coronacollina acula, described by Clites and colleagues (27), is preserved in the Ediacara Member (Rawnsley Quartzite) of South Australia and represents the oldest multielement organism (Fig. 3). Coronacollina consists of a triradial truncated cone associated with ruler-straight spicules, up to 37 cm in length, diverging radially from the cone. The spicules most commonly disarticulated after death and only rarely are found attached to the truncated cone.

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Fig. 3.

C. acula represents the oldest evidence of skeletonization. (A) A reconstruction of C. acula, after Clites and colleagues (27). This reconstruction is based on known specimens that have only up to four spicules, but it is likely it had more. (B) The holotype SAM P43257 of C. acula. The central depression is the mold of the thimble-like main body of the specimen. Note the rigid spicules that radiate from the main body.

The morphologic consistency between articulated and disarticulated spicules suggests they were made of a rigid substance, such as opaline silica or calcium carbonate. In life, the spicules likely provided structural support in a manner similar to the Cambrian demosponge, Choia. Although generally preserved flattened, Choia specimens from the Cambrian Fezouata Formation of Morocco exhibit raised central regions, perhaps representing soft tissue replaced by pyrite. The presence of Ediacaran sponge-grade organisms has been suggested by both biomarkers (52) and other body fossils. A recent review questions the Poriferan origin of many of these taxa, suggesting that some are, for example, holdfasts or microbial in origin (53). However, the sharply preserved spiculate structures and the nature of preservation in some of these taxa such as Paleophragmodictya cannot be easily reconciled with organic fibers, tentacles, or microbial structures or a holdfast origin. Constructed from a framework of rigid and brittle elements, Coronacollina reveals a constructional mode only recently recognized among members of the Ediacara biota. It provides a link in constructional mode across the Cambrian boundary and sheds light on the development of structural support in early sponges. Although in many respects morphologically simple, Coronacollina is nonetheless one of the most complicated of the Ediacara taxa because it was composed of at least two different materials: the soft-bodied truncated cone, which was solid enough to withstand compaction, and biomineralized spicules.

Mobility and the Presence of Bilaterians

The majority of organisms comprising the Ediacara Biota are interpreted to represent stationary or attached organisms. However, it now appears that at least four different Ediacaran organisms were capable of movement. The association of certain body fossil taxa with motility and feeding traces provides the earliest evidence that the Ediacara Biota included bilaterian-grade animals. External molds of Kimberella (Fig. 1D) have been documented in close association with casts of arrays of fanned sets of bifid scratch traces (Kimberichnus teruzzii; Fig. 1F) from the Ediacara Member of the Rawnsley Quartzite, South Australia, and the Verkhovka Formation, Zimnie Gory Formation, and in the basal part of the Erga Formation of the White Sea region of northwestern Russia. From their orientation and proximity, these body and trace fossils are interpreted as evidence of mat grazing activities (31, 54, 55). The suggestions of molluscan affinities for Kimberella (23, 24, 53) should not overlook some important differences from extant gastropod grazing behaviors (31, 56). Two genera of the so-called dickinsoniomorphs, Dickinsonia (Fig. 1A) and Yorgia, are preserved as external molds at the end of serial sets of roughly oriented faint casts of what are interpreted as “resting” or “feeding” traces, where these organisms remained stationary for periods of time, decomposing the microbial mat substrate, before moving to the next site, until the sediment-smothering events that preserved them and their “footprints” (57). Suggestions that these are evidence of fungal “fairy-rings” (58), or random products of wave or current transport (59), are easily countered by the repeated observation that the “footprints” were made in a definite order, as determined by identification of the body axis and anterior enlargement of body divisions in these organisms. The implication that the mat on the substrate decomposed sufficiently to enable a cast suggests that such a process could have been a source of nutrition for dickinsoniids. Alone among the Ediacara biota, dickinsoniids feature preserved external body molds with apparent contraction marks and variable patterns of body divisions that might be explained by muscular peristaltic contraction. There is no equivalent evidence of differential contraction of body elements among the array of taxa of Petalonamae, such as Pteridinium (Fig. 1H) and Phyllozoon (9).

The most abundant trace fossils in shallow marine environments associated with rich assemblages of the Ediacara Biota are very common groove and levee trails of Helminthoidichnites (Fig. 1I) that are found in both part and counterpart on numerous bedding surfaces with or without body fossil impressions. Uniquely, Helminthoidichnites is preserved on bed soles as groove and levee and shows alternation of relief, but only when the sandstone layer is less than 15 mm thick and not covering an entire bed. This association is interpreted as a product of mat mining by an animal too small to be characterized from casts and molds and limited by the redox state within partly buried mat substrates. On the basis of fine-grained sandy layers, scalloped levees enable the direction of burrowing to be determined (Fig. 1I, Upper Left). On bed tops, Helminthoidichnites displays evidence of avoidance behavior exhibited by parallel spirals and changing depth where crossings occurred. These traces are common in the younger Ediacaran formations from relatively shallower-water environments such as the Ediacara Member of the Rawnsley Quartzite in South Australia (19), the Blueflower Formation of the Mackenzie Mountains of northwest Canada (60), and the Shibantan Member of the Dengjing Formation in south China (61, 62). It is unlikely these complicated but definitive trace fossils could have been made by anything other than a bilaterian.

The serial arcuate looping forms, Paleopascichnus and Yelovichnus, and chains hemispheres, referred to as Neonereites, are now considered encrusting body fossils, reinterpreted as xenophyophores by Seilacher and colleagues (63), but disputed by Antcliffe and colleagues (64). The oldest described trace fossils seem to be those of actinian-grade polyps that left simple straight or curved locomotive trails in ash-coated, deep-water substrates in the Mistaken Point Formation assemblage in southeastern Newfoundland (65).

Concluding Remarks

Taken as a whole, the Ediacara Biota represents an enigmatic assemblage of fossils that are not easily related to modern taxa. However, examination of aspects of the ecology, such as trace fossils, taphonomy, and morphology, reveal that these fossils show characteristics of modern taxa. It is clear that bilaterians, cnidarians, and poriferans are represented among the Ediacara Biota. Although we may never be able to reconcile the phylogeny of all, or even most, of the Ediacara taxa, it is likely that with these approaches, we will be able to continue to better relate these taxa with both modern and extinct animals.